Elucidating the role of the gut microbiota in the physiological effects of dietary fiber

Edward C. Deehan; Zhengxiao Zhang; Alessandra Riva; Anissa M. Armet; Maria Elisa Perez-Muñoz; Nguyen K. Nguyen; Jacqueline A. Krysa; Benjamin Seethaler; Yuan Yuan Zhao; Janis Cole; Fuyong Li; Bela Hausmann; Andreas Spittler; Julie Anne Nazare; Nathalie M. Delzenne; Jonathan M. Curtis; Wendy V. Wismer; Spencer D. Proctor; Jeffrey A. Bakal; Stephan C. Bischoff; Dan Knights; Catherine J. Field; David Berry; Carla M. Prado; Jens Walter

doi:10.1186/s40168-022-01248-5

Elucidating the role of the gut microbiota in the physiological effects of dietary fiber

Edward C. Deehan, Zhengxiao Zhang, Alessandra Riva, Anissa M. Armet, Maria Elisa Perez-Muñoz, Nguyen K. Nguyen, Jacqueline A. Krysa, Benjamin Seethaler, Yuan Yuan Zhao, Janis Cole, Fuyong Li, Bela Hausmann, Andreas Spittler, Julie Anne Nazare, Nathalie M. Delzenne, Jonathan M. Curtis, Wendy V. Wismer, Spencer D. Proctor, Jeffrey A. Bakal, Stephan C. BischoffDan Knights, Catherine J. Field, David Berry, Carla M. Prado, Jens Walter

Research output: Contribution to journal › Article › peer-review

41 Scopus citations

Abstract

BACKGROUND: Dietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25-35 kg/m 2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers.

RESULTS: AX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC.

CONCLUSION: This study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization.

TRIAL REGISTRATION: Clinicaltrials.gov, NCT02322112 , registered on July 3, 2015. Video Abstract.

Original language	English (US)
Article number	77
Journal	Microbiome
Volume	10
Issue number	1
DOIs	https://doi.org/10.1186/s40168-022-01248-5
State	Published - Dec 2022

Bibliographical note

Funding Information:
We thank AgriFiber Solutions LLC (Illinois, USA) for providing AGRIFIBER SFC, and Blanver Farmoquimica LTDA (São Paulo, Brazil) for providing MICROCEL MC-12. We also thank Petra Pjevac, Jasmin Schwarz, and Gudrun Kohl from the Joint Microbiome Facility (Vienna, Austria) for supporting the ex vivo microbiota analysis.

Funding Information:
This study was co-funded by a joint European Research Area and Joint Programming Initiative-A Healthy Diet for a Healthy Life (ERA-HDHL) grant (Biomarkers for Nutrition and Health; The FiberTAG Project; www.healthydietforhealthylife.eu/ ) with specific contributions from the Canadian Institutes of Health Research (RN-298871-372173). The ex vivo microbiota analysis was supported by the European Research Council (Starting Grant: FunKeyGut 741623). ECD acknowledges support from the Queen Elizabeth II Graduate Scholarship, Elizabeth Russell MacEachran Scholarship, and Anthony Fellowship in Human Nutrition. JW is funded in part by a Science Foundation Ireland Centre grant to APC Microbiome Ireland (APC/SFI/12/RC/2273_P2) and a Science Foundation Ireland Professorship (19/RP/6853). The funding sources had no role in study design, data collection and analysis, decision to publish, or manuscript preparation.

Publisher Copyright:
© 2022, The Author(s).

Keywords

Adults
Dietary fiber
Gut microbiota
Inflammation
Insulin resistance
Obesity
Satiety
Biomarkers/analysis
Humans
Bile Acids and Salts/analysis
Obesity/microbiology
Male
Leukocyte L1 Antigen Complex/analysis
Feces/microbiology
Gastrointestinal Microbiome/physiology
Adult
Bacteria
Dietary Fiber
Female

PubMed: MeSH publication types

Clinical Trial
Research Support, Non-U.S. Gov't
Video-Audio Media
Journal Article

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Publisher link

10.1186/s40168-022-01248-5

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Deehan, E. C., Zhang, Z., Riva, A., Armet, A. M., Perez-Muñoz, M. E., Nguyen, N. K., Krysa, J. A., Seethaler, B., Zhao, Y. Y., Cole, J., Li, F., Hausmann, B., Spittler, A., Nazare, J. A., Delzenne, N. M., Curtis, J. M., Wismer, W. V., Proctor, S. D., Bakal, J. A., ... Walter, J. (2022). Elucidating the role of the gut microbiota in the physiological effects of dietary fiber. Microbiome, 10(1), Article 77. https://doi.org/10.1186/s40168-022-01248-5

Deehan, EC, Zhang, Z, Riva, A, Armet, AM, Perez-Muñoz, ME, Nguyen, NK, Krysa, JA, Seethaler, B, Zhao, YY, Cole, J, Li, F, Hausmann, B, Spittler, A, Nazare, JA, Delzenne, NM, Curtis, JM, Wismer, WV, Proctor, SD, Bakal, JA, Bischoff, SC, Knights, D, Field, CJ, Berry, D, Prado, CM & Walter, J 2022, 'Elucidating the role of the gut microbiota in the physiological effects of dietary fiber', Microbiome, vol. 10, no. 1, 77. https://doi.org/10.1186/s40168-022-01248-5

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abstract = "BACKGROUND: Dietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25-35 kg/m 2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers. RESULTS: AX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC.CONCLUSION: This study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization.TRIAL REGISTRATION: Clinicaltrials.gov, NCT02322112 , registered on July 3, 2015. Video Abstract.",

keywords = "Adults, Dietary fiber, Gut microbiota, Inflammation, Insulin resistance, Obesity, Satiety, Biomarkers/analysis, Humans, Bile Acids and Salts/analysis, Obesity/microbiology, Male, Leukocyte L1 Antigen Complex/analysis, Feces/microbiology, Gastrointestinal Microbiome/physiology, Adult, Bacteria, Dietary Fiber, Female",

author = "Deehan, {Edward C.} and Zhengxiao Zhang and Alessandra Riva and Armet, {Anissa M.} and Perez-Mu{\~n}oz, {Maria Elisa} and Nguyen, {Nguyen K.} and Krysa, {Jacqueline A.} and Benjamin Seethaler and Zhao, {Yuan Yuan} and Janis Cole and Fuyong Li and Bela Hausmann and Andreas Spittler and Nazare, {Julie Anne} and Delzenne, {Nathalie M.} and Curtis, {Jonathan M.} and Wismer, {Wendy V.} and Proctor, {Spencer D.} and Bakal, {Jeffrey A.} and Bischoff, {Stephan C.} and Dan Knights and Field, {Catherine J.} and David Berry and Prado, {Carla M.} and Jens Walter",

note = "Funding Information: We thank AgriFiber Solutions LLC (Illinois, USA) for providing AGRIFIBER SFC, and Blanver Farmoquimica LTDA (S{\~a}o Paulo, Brazil) for providing MICROCEL MC-12. We also thank Petra Pjevac, Jasmin Schwarz, and Gudrun Kohl from the Joint Microbiome Facility (Vienna, Austria) for supporting the ex vivo microbiota analysis. Funding Information: This study was co-funded by a joint European Research Area and Joint Programming Initiative-A Healthy Diet for a Healthy Life (ERA-HDHL) grant (Biomarkers for Nutrition and Health; The FiberTAG Project; www.healthydietforhealthylife.eu/ ) with specific contributions from the Canadian Institutes of Health Research (RN-298871-372173). The ex vivo microbiota analysis was supported by the European Research Council (Starting Grant: FunKeyGut 741623). ECD acknowledges support from the Queen Elizabeth II Graduate Scholarship, Elizabeth Russell MacEachran Scholarship, and Anthony Fellowship in Human Nutrition. JW is funded in part by a Science Foundation Ireland Centre grant to APC Microbiome Ireland (APC/SFI/12/RC/2273_P2) and a Science Foundation Ireland Professorship (19/RP/6853). The funding sources had no role in study design, data collection and analysis, decision to publish, or manuscript preparation. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1186/s40168-022-01248-5",

language = "English (US)",

volume = "10",

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T1 - Elucidating the role of the gut microbiota in the physiological effects of dietary fiber

AU - Deehan, Edward C.

AU - Zhang, Zhengxiao

AU - Riva, Alessandra

AU - Armet, Anissa M.

AU - Perez-Muñoz, Maria Elisa

AU - Nguyen, Nguyen K.

AU - Krysa, Jacqueline A.

AU - Seethaler, Benjamin

AU - Zhao, Yuan Yuan

AU - Cole, Janis

AU - Li, Fuyong

AU - Hausmann, Bela

AU - Spittler, Andreas

AU - Nazare, Julie Anne

AU - Delzenne, Nathalie M.

AU - Curtis, Jonathan M.

AU - Wismer, Wendy V.

AU - Proctor, Spencer D.

AU - Bakal, Jeffrey A.

AU - Bischoff, Stephan C.

AU - Knights, Dan

AU - Field, Catherine J.

AU - Berry, David

AU - Prado, Carla M.

AU - Walter, Jens

N1 - Funding Information: We thank AgriFiber Solutions LLC (Illinois, USA) for providing AGRIFIBER SFC, and Blanver Farmoquimica LTDA (São Paulo, Brazil) for providing MICROCEL MC-12. We also thank Petra Pjevac, Jasmin Schwarz, and Gudrun Kohl from the Joint Microbiome Facility (Vienna, Austria) for supporting the ex vivo microbiota analysis. Funding Information: This study was co-funded by a joint European Research Area and Joint Programming Initiative-A Healthy Diet for a Healthy Life (ERA-HDHL) grant (Biomarkers for Nutrition and Health; The FiberTAG Project; www.healthydietforhealthylife.eu/ ) with specific contributions from the Canadian Institutes of Health Research (RN-298871-372173). The ex vivo microbiota analysis was supported by the European Research Council (Starting Grant: FunKeyGut 741623). ECD acknowledges support from the Queen Elizabeth II Graduate Scholarship, Elizabeth Russell MacEachran Scholarship, and Anthony Fellowship in Human Nutrition. JW is funded in part by a Science Foundation Ireland Centre grant to APC Microbiome Ireland (APC/SFI/12/RC/2273_P2) and a Science Foundation Ireland Professorship (19/RP/6853). The funding sources had no role in study design, data collection and analysis, decision to publish, or manuscript preparation. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - BACKGROUND: Dietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25-35 kg/m 2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers. RESULTS: AX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC.CONCLUSION: This study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization.TRIAL REGISTRATION: Clinicaltrials.gov, NCT02322112 , registered on July 3, 2015. Video Abstract.

AB - BACKGROUND: Dietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25-35 kg/m 2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers. RESULTS: AX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC.CONCLUSION: This study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization.TRIAL REGISTRATION: Clinicaltrials.gov, NCT02322112 , registered on July 3, 2015. Video Abstract.

KW - Adults

KW - Dietary fiber

KW - Gut microbiota

KW - Inflammation

KW - Insulin resistance

KW - Obesity

KW - Satiety

KW - Biomarkers/analysis

KW - Humans

KW - Bile Acids and Salts/analysis

KW - Obesity/microbiology

KW - Male

KW - Leukocyte L1 Antigen Complex/analysis

KW - Feces/microbiology

KW - Gastrointestinal Microbiome/physiology

KW - Adult

KW - Bacteria

KW - Dietary Fiber

KW - Female

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Elucidating the role of the gut microbiota in the physiological effects of dietary fiber

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

UN SDGs

Publisher link

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